An Old World leaf-cutting, fungus-growing ant: A case of convergent evolution

Ecol Evol. 2023 Mar 15;13(3):e9904. doi: 10.1002/ece3.9904. eCollection 2023 Mar.

Abstract

The African myrmicine ant Crematogaster clariventris is a territorially dominant arboreal species that constructs very hard carton nests. Noting that workers cut off leaves from different plant species while building or repairing their nests, we asked ourselves if there was a correlation. We conducted scanning electron microscopic observations of nest walls that revealed the presence of fungal mycelia. As the presence of filamentous Ascomycota has been shown on arboreal ant nests worldwide, we used a metabarcoding approach and, indeed, noted the presence of Operational Taxonomic Unit (OTU) Cre_006041 of the Capnodiales known to reinforce large nests of an unidentified African Crematogaster. This OTU was also recorded in the workers' bodies. At a very low level, we also noted OTU Cre_320021 of the Chaetothyriales known for their relationships with the African plant-ant species C. margaritae. Therefore, by cutting leaves and growing fungus, C. clariventris illustrates a case of convergent evolution with higher New World leaf-cutting, fungus-growing Attina of the genera Acromyrmex, Amoimyrmex and Atta. However, there are notable differences. Leaf-cutting Attina cultivate Agaricaceae (Basidiomycota) for food, whereas C. clariventris uses Capnodiales to reinforce their nests (i.e., after the mycelium died, the hyphae's cell walls remained sturdy forming a natural composite material), have a distinct geographical origin (i.e., New World vs. Old World) and belong to a distinct ant tribe in the subfamily Myrmicinae (i.e., Attini vs. Crematogastrini). Furthermore, leaf-cutting Attina evolved an efficacious means of cutting leaves by using their mandibles asymmetrically, whereas C. clariventris workers, typically, use their mandibles symmetrically.

Keywords: Crematogaster; ant–fungus relationships; carton nest structure; defoliation; evolution; mycelium‐composite material.

Associated data

  • figshare/10.6084/m9.figshare.14452692.v5